Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 DOI 10.1186/s40249-015-0072-y

RESEARCH ARTICLE Open Access Annual trends of human brucellosis in pastoralist communities of south-western : a retrospective ten-year study Catherine Kansiime1*, Elizeus Rutebemberwa1, Benon B. Asiimwe2, Fredrick Makumbi3, Joel Bazira4 and Anthony Mugisha5

Abstract Background: Human brucellosis is prevalent in both rural and urban Uganda, yet most cases of the disease in humans go unnoticed and untreated because of inaccurate diagnosis, which is often due to the disease not manifesting in any symptoms. This study was undertaken to describe trends in laboratory-confirmed human brucellosis cases at three health facilities in pastoralist communities in South-western, Uganda. Methods: Data were collected retrospectively to describe trends of brucellosis over a 10-year period (2003–2012), and supplemented with a prospective study, which was conducted from January to December 2013. Two public health facilities and a private clinic that have diagnostic laboratories were selected for these studies. Annual prevalence was calculated and linearly plotted to observe trends of the disease at the health facilities. A modified Poisson regression model was used to estimate the risk ratio (RR) and 95 % confidence intervals (CIs) to determine the association between brucellosis and independent variables using the robust error variance. Results: A total of 9,177 persons with suspected brucellosis were identified in the retrospective study, of which 1,318 (14.4 %) were confirmed cases. Brucellosis cases peaked during the months of April and June, as observed in nearly all of the years of the study, while the most noticeable annual increase (11–23 %) was observed from 2010 to 2012. In the prospective study, there were 610 suspected patients at two public health facilities. Of these, 194 (31.8 %) were positive for brucellosis. Respondents aged 45–60 years (RR = 0.50; CI: 0.29–0.84) and those that tested positive for typhoid (RR = 0.68; CI: 0.52–0.89) were less likely to have brucellosis. Conclusions: With the noticeable increase in prevalence from 2010 to 2012, diagnosis of both brucellosis and typhoid is important for early detection, and for raising public awareness on methods for preventing brucellosis in this setting. Keywords: Trends, Brucellosis, Pastoralist communities

Background The most recent review of the disease indicates that the Brucellosis is considered to be the most common zoo- highest incidence of brucellosis in Africa was recorded notic infection worldwide [1], with more than 500,000 in Algeria at 84.3 per million of population per year, and cases recorded annually [2, 3]. In Africa, especially south the lowest in Uganda at 0.9 per million of population of the Sahara, many of the known zoonotic diseases – per year. The disease is known to be endemic in including brucellosis – commonly occur and are poorly Cameroon and Ethiopia, but no specific data is available controlled in both humans and domesticated animals. for these countries [1]. In Sub-Saharan Africa, most human cases of brucellosis go unnoticed and untreated because of inaccurate diagno- * Correspondence: [email protected] sis, which is often due to the disease not manifesting in 1Department of Health Policy, Planning and Management, School of Public Health, College of Health Sciences, Makerere University, P.O. Box 7072, any specific symptoms. This makes it difficult to clinically , Uganda distinguish brucellosis from typhoid, rheumatic fever, joint Full list of author information is available at the end of the article

© 2015 Kansiime et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 2 of 8

diseases and malaria [4]. For this reason, official figures do referral hospital in the former headquarters of . not fully reflect the actual burden, and the World Health The private clinic was chosen because it had detailed Organization estimates that the true incidence of the dis- records of patients that attended the clinic during our ease in developing countries may be between 10 and 25 study period and had many referred patients from times higher than what reported figures indicate [5]. With . its diverse clinical manifestations, human brucellosis can All the districts in the study area are mainly comprised only be proven by laboratory diagnosis. populations whose livelihoods depend on cattle as well In Uganda, human brucellosis has been reported to as other animal products for food and trade. They are: be prevalent in both rural and urban settings [6, 7]. A farmers who are settled and solely grow crops (mostly recent study revealed that 12.6 % of informally mar- recent migrants to the area), agro-pastoralists who rear keted milk in urban Kampala was contaminated with cattle as well as practice farming, and pure pastoralists Brucella abortus at purchase; and that the annual hu- or semi-nomads who rear cattle but have permanent man incidence rate was estimated to be 5.8 per 10,000 shelters, moving their animals in dry seasons in search people [8]. Studies on animal brucellosis have also been of water and pasture. The District neighbours done in Uganda, reporting a herd prevalence of 55.6 % the , a predominantly cattle keeping and an animal prevalence of 15.8 % in the pastoral area, and was therefore purposively selected to capture dairy system in the [9], while higher that population. This hospital receives patients from figures of up to 100 % at herd level and 30 % at animal both the Lyantonde and Kiruhura districts, as well as level were reported in the central district of Nakasongola neighbouring areas. [10]. Brucellosis is also prevalent among Ugandan wildlife [11]. Pastoral communities in Uganda are commonly found living on the periphery, adjacent to wildlife conser- Study design vation parks. Additionally, their close contact with cattle, A retrospective study was conducted from January as well as their love for consuming raw milk and fermen- 2003 to December 2012, inclusive, in order to describe ted milk products exposes them to brucellosis. While trends in the prevalence of brucellosis over a 10-year health education and promotion outreach programmes period. This was done by reviewing serological reports are conducted in such communities, it is not known if at the teaching hospital and the they are successful. Conducting a trends analysis is im- Mbarara diagnostic clinic. This was also supplemented portant to assess the effectiveness of such programmes. by a 1-year prospective study (January to December The objective of this study was to describe trends in 2013), which was conducted at the Mbarara University laboratory-confirmed human brucellosis cases at two teaching hospital and Lyantonde hospital in order to fill public hospitals and a private clinic in the Mbarara and the gaps of the retrospective study. Lyantonde districts, in southwestern Uganda. We en- visage that the data obtained will inform public health efforts for the design of effective health education pro- Data collection grammes and development of control strategies against For both the retrospective and prospective studies, brucel- brucellosis in the country. losis test results and socio-demographic data of the pa- tients were obtained from laboratory records. The selected laboratories in these studies follow a standard operating Methods procedure recommended by the Ministry of Health, Study setting Uganda. Records were searched for all suspected cases Our study was conducted at three health facilities that that presented to the selected clinics during the period have the capacity to diagnose and treat brucellosis: two between January 2003 and December 2012. During the public laboratories (the Mbarara University teaching prospective study, patients took brucellosis tests (January hospital and the Lyantonde hospital), and a private clinic to December 2013). Recommendation by a clinician to (the Mbarara diagnostic clinic). The retrospective study test for brucellosis was based on the presence of clin- focused on the Mbarara University teaching hospital ical signs and symptoms of fever, sweating, fatigue and and Mbarara diagnostic clinic, which are situated less other symptoms as defined by the Centers for Disease than 1 km apart. These were purposively selected Control and Prevention [12]. Individual information on because the teaching hospital serves as the referral sex, age, area of residence, month of diagnosis and hospital for five districts that were formerly part of the antibody titres were obtained. Serological testing was Greater Mbarara District before it was divided into five done at the hospitals by the plate agglutination test, smaller districts (Isingiro, Kiruhura, Kazo, Ibanda and which has a sensitivity and specificity of 0.771 and Mbarara). The people in these districts still access the 0.960, respectively [13]. Uganda is considered a low Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 3 of 8

prevalence setting [1], therefore a dilution titre of Results ≥1:80 of the diagnostic test was considered positive for Participant characteristics the disease [14]. In the retrospective study, a total of 9,177 suspects (4,209 males and 4,968 females) presented to the health facilities with symptoms suggestive of brucellosis and Data analysis were serologically tested. A total of 1,318 cases of bru- The annual prevalence rates were calculated based on the cellosis were identified using a cut-off of ≥1:80; of these, number of cases in the three laboratories as a ratio of the 207 (15.7 %) were diagnosed at the Mbarara University annual total population at risk in each facility, expressed teaching hospital, while 1,111 (84.3 %) were diagnosed at as a percentage. The annual prevalence of human brucel- the private clinic. At the teaching hospital, the number losis in both studies was calculated. Descriptive analysis of cases per year increased from five (12.8 %) in 2003 to was conducted for retrospective data and linearly plotted 17 (12.5 %) in 2004 to 24 (14.4 %) in 2007, with the to observe the trends of the disease. We stratified the ana- highest prevalence of 42 cases (30 %) recorded in 2012. lysis by health facility for the retrospective study in order At the private clinic, the number of cases noticeably to compare trends of brucellosis at a private and a public increased from two in 2004 to 77 in 2007, with a peak of facility, as well as to guide us in future recommendations 339 cases in 2012, and corresponding prevalence of for disease control. Prospective data were analysed with 2.7 %, 17 % and 21.3 %, respectively. The most notice- Stata (Stata Corp LP, Texas, USA) version 12 statistical able annual increase in prevalence at both facilities was software package. Chi-square tests were used for cat- observed from 2010 to 2012, with records showing a egorical variables. At bivariate analysis, categorical vari- change from 13 (8.2 %) to 42 (30 %) cases at the teach- ables including age, sex, occupation, area of residence, ing hospital (see Fig. 1), and 144 (9.9 %) to 339 (21.3 %) health facility, symptoms of brucellosis, and whether tests cases at the private clinic. for other diseases such as malaria and typhoid were con- In the prospective study, a total of 610 participants ducted were assessed for the association between the inde- presented with symptoms suggestive of brucellosis be- pendent variables and presence or absence of brucellosis. tween January and December 2013, inclusive. Of these, The prospective categorical data were compared using 228 (37.4 %) were from Mbarara University teaching the chi-square test and p ≤ 0.05 was considered statisti- hospital, while 382 (62.6 %) were from Lyantonde hos- cally significant. We used a modified Poisson regression pital. Of the 610 participants, 194 (31.8 %) tested positive model with a robust error variance to estimate the risk for brucellosis; 66 (34 %) were from Mbarara hospital and ratio (RR) and 95 % confidence intervals (CIs) to deter- 128 (66 %) were from Lyantonde hospital. The annual mine the association between the presence or absence of brucellosis prevalence was calculated as the total num- brucellosis and the independent variables. The advantage ber of cases in a given year divided by the total number of using RR is that it narrows the CIs and is preferred of population at risk per year at the hospitals. At the over the odds ratio for prospective investigations [15]. Mbarara hospital, the prevalence was 66/128 (51.6 %), The additional advantage of estimating relative risk by while at the Lyantonde hospital it was 128/382 (33.5 %). using a logarithm link is that the estimates are relatively robust to omitted covariates [16], in contrast to logistic regression. We adjusted the RR for other predictors or Gender distribution of cases potential confounders (age and occupation) by adding From the 1,318 brucellosis cases observed during the them to the model that had variables with p ≤0.2, as de- retrospective study, 560 were male (42.5 %) patients and termined by the bivariate analysis. 758 were female (57.5 %). To break this down further by facility, 76 (36.7 %) males and 131 (63.3 %) females were infected at the teaching hospital, while 481 (43.3 %) males Ethical considerations and 630 (56.7 %) females were infected at the private The study protocol was approval by the Makerere Univer- clinic. There was no significant difference in the number sity School of Public Health Higher Degrees, Research and of cases by gender (p = 0.34) at both health facilities. How- Ethics Committee, and the Uganda National Council of ever, there was a significant difference (p <0.001)inthe Science and Technology. The study objective was ex- number of cases diagnosed at the two health facilities, plained to the directors of the hospitals and the technical with the private clinic diagnosing more cases than the staff (laboratory technicians, clinicians and nurses), while public hospital. informed written consent was obtained from each partici- Of the 610 participants in the prospective study, 213 pant in his/her local language. Data collected were coded were males (34.9 %) and 397 were females (65.1 %). Of for anonymity, and confidentiality was assured at all stages the 397 females, 144 (36.3 %) were from the Mbarara of the study. hospital and 253 (63.7 %) were from Lyantonde hospital. Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 4 of 8

Fig. 1 Annual trends of human brucellosis prevalence at Mbarara teaching hospital (MH) and Mbarara diagnostic clinic (MD) from 2003 to 2012

The infection rates among males and females at the diagnosed at the two health facilities (p = 0.22), as shown Mbarara hospital were 22/66 (33.3 %) and 44/66 by the chi-square test. (66.7 %), while at the Lyantonde hospital they were 38/ 128 (29.7 %) and 90/128 (70.3 %), respectively. There Seasonal variation of cases were no significant differences between genders and Descriptive analysis using graphs was used to show health facilities (p = 0.44), or in the number of cases seasonal variations. The peak of brucellosis cases in the

Fig. 2 The seasonal distribution of human brucellosis at the two health facilities (Mbarara teaching hospital and Mbarara diagnostic clinic), 2003–2012 Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 5 of 8

10-year study was observed during the months of April Factors associated with brucellosis (prospective study) and June at both health facilities. Cases at the private clinic The variables that were taken for the multivariate ana- increased during October, November and December, while lysis were age, sex, occupation, health facility, symptoms at the teaching hospital, a marked decrease was observed of brucellosis, and whether tests were done for malaria inthesametimeperiod(seeFig.2). and typhoid. The multivariate analysis showed that The prospective study showed that there was a signifi- people with occupations such as business owner, civil cant difference in the number of cases presented at the servant or self-employed (RR =0.29; CI: 0.11–0.82) were health facilities (p < 0.001), with more cases observed at less likely to have brucellosis compared to farmers and the Lyantonde hospital. At the Mbarara University pastoralists. We adjusted the RRs for other predictors teaching hospital, cases increased in the months of and potential confounders by adding them to the model. February to March, May to August, and October to There were no confounding differences observed. Add- November, while at the Lyantonde hospital, cases in- itionally, respondents aged 45–60 years (RR = 0.50; CI: creased in the months of January to February, May to 0.29–0.84) were less likely to have brucellosis compared July, and September to November (see Fig. 3). A steady to the other age groups, and those that tested positive increase was observed at Lyantonde in May to July and at for typhoid (RR = 0.68; CI: 0.52–0.89) were less likely to Mbarara in May to August (see Fig. 3). A decrease in the have brucellosis compared to those who tested negative number of cases was observed in the months of April to (see Table 1). May and November to December at both hospitals. A significant difference was observed between the health facilities and the months with the highest incidence of Discussion cases, with a p <0.001. The results of our retrospective study showed that the trend distribution of human brucellosis in the study area varied in different years, with the most noticeable Symptoms of brucellosis increase in prevalence recorded from 2010 to 2012 at During the prospective study, data were collected on pa- both health facilities; from 13 (8.2 %) to 42 (30 %) cases tients’ symptoms at presentation to the health facility. The at the teaching hospital, and 144 (9.9 %) to 339 (21.3 %) major symptoms reported were: headaches 415/610 cases at the private clinic. A probable explanation for (68 %), joint pains 401 (65.7 %), general weakness 331 this increase is that health education about brucellosis (54.3 %) and recurrent fever 323 (53 %). Other symptoms and other zoonotic diseases has been provided through mentioned were weight loss, loss of appetite and sweats. local radio stations in this setting. Therefore, these

Fig. 3 Monthly trends of brucellosis at the Mbarara teaching hospital (MH) and Lyantonde hospital (LH) in 2013 Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 6 of 8

Table 1 Multivariate analysis showing factors associated with brucellosis during the prospective study (January 2013 – February 2013) Brucellosis results, n (%) Unadjusted RR(95 % CI) Adjusted RR(95 % CI) P-value Variables Negative 416(68.2 %) Positive 194(31.8 %) Age 0–18 38(9.1) 23(11.9) 1 1 19–30 168(40.4) 76(39.2) 0.83(0.57–1.20) 0.77(0.53–1.12) 0.18 31–45 128(30.8) 69(35.6) 0.94(0.65–1.37) 0.86(0.58–1.26) 0.44 46–60 65(15.6) 17(8.8) 0.54(0.32–0.94) 0.50(0.29–0.84) 0.01* +61 17(4.1) 9(4.6) 0.92(0.49–1.70) 0.83(0.45–1.51) 0.54 Sex Male 153(36.8) 60(30.9) 1 1 Female 263(63.2) 134(69.1) 1.21(0.93–1.57) 0.81(0.63–1.04) 0.10 Occupation Farmer 142(34.1) 68(35.1) 1 1 Agro-pastoralist 66(15.9) 41(21.1) 1.17(0.86–1.59) 0.81(0.48–1.38) 0.44 Pastoralists 14(3.4) 9(4.6) 1.19(0.69–2.05) 0.89(0.52–1.53) 0.68 Others 194(46.6) 76(39.2) 0.85(0.65–0.12) 0.66(0.39–1.12) 0.12 Malaria results Negative 381(91.6) 166(85.6) 1 1 Positive 35(8.4) 28(14.4) 0.94(0.56-1.03) 2.29(0.68–1.31) 0.73 Typhoid test Negative 405(97.4) 120(61.9) 1 1 Positive 11(2.6) 74(38.1) 0.67(0.53–0.87) 0.68(0.52–0.89) <0.005* RR Risk ratio * means level of significance <0.05 awareness campaigns may be credited with helping to For instance, reported incidences are; the most recent improve health-seeking behaviour, meaning more people review [1] that indicates the highest incidence of bru- present to health facilities to get tested. In contrast, a cellosis in Africa was recorded in Algeria at 84.3 per 24-year trend study conducted in Saudi Arabia found a million of population per year and the lowest was in decreasing incidence rate of disease from 26.3/100,000 Uganda at 0.9 per million of population per year. in 1983–1992 to 6/100,000 in 1993–2007 [17] as a result Therefore, there is a need to provide diagnostic tests of effective control measures in animals [18]. Therefore, and ensure the availability of brucellosis treatment for in order to reduce brucellosis in humans, the disease patients, as early diagnosis and prompt treatment is es- should first be controlled in animals as they are the res- sential in preventing complications and relapses. ervoirs of the disease [19]. This can be achieved through In both the retrospective and prospective studies, there health education, community sensitisation and animal were more females diagnosed with brucellosis than vaccination. males, however, we found no significant difference be- The annual prevalence of human brucellosis in 2012 tween gender and having the disease at the bivariate was 30 and 21.3 % at the Mbarara teaching hospital and analysis. A study in Kampala found that being female private clinic, respectively. During the 1-year prospective was a risk factor for brucellosis seropositivity [7]. This study, the annual prevalence was 51.6 and 33.5 % at the finding may be attributed to the specific gender roles in Mbarara teaching hospital and Lyantonde hospital, re- households in this setting. For example, females in our spectively. This depicts a high prevalence of the disease study area are more involved in the handling of milk at these facilities. Elsewhere, in Chad [20], prevalence and other dairy products, which are transmission routes of human brucellosis among nomadic pastoralists was for the disease. Similar findings have been reported in reported at 3.8 % in 2003, a much smaller prevalence. the United Kingdom and India [3, 19]. On the other However, more often than not, it is the incidence of hand, studies in Saudi Arabia, Greece and Tanzania have brucellosis that is reported, not the prevalence, which found that being male is related to risk of occupational may not be an accurate representation of the situation. exposure [17, 21, 22]. These disparities in gender are Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 7 of 8

most likely related to the differences in practices, habits compared to other age groups. This could be because the and occupations of the study populations, where for health facilities where the study was conducted receives example, women handle dairy products while men han- patients from a wide range of communities, not necessar- dle meat and assist in the delivery of animals. There is a ily pastoralists. However, a study done in Germany [23] on need to study gender relations at household level in bru- changing epidemiology of human brucellosis in laboratory cellosis endemic areas. This will enable researchers to diagnostic setting (1962–2005) found that age-specific identify areas on which to focus health education efforts incidence was highest for persons aged 60–69 years. An- and risk factor assessment in order to control the disease other study done in Saudi Arabia showed that the high- in humans in Uganda. est rate of brucellosis was in patients aged 40–49 years Cases of brucellosis peaked during the months of April (100/100,000). and June at both health facilities in almost every year of In addition, respondents whose occupations were busi- the retrospective study. This finding is similar to a study ness owners, civil servants or who were self-employed conducted in Saudi Arabia, which also observed the were less likely to have brucellosis compared to agro- highest number of cases from April to June [17]. Fur- pastoralists and farmers. This could be because these thermore, we observed an increase in cases in the months occupations do not require being in close proximity with of October to December at the private clinic, but cases animals, as compared to pastoralists. The pastoralists’ high were remarkably reduced during the same months at the consumption of raw milk and fresh cheese is another teaching hospital. The increase of cases might be due to factor [25]. There is a need to continuously sensitise all the relationship between milk yields and rainfall as previ- agricultural and pastoral occupations about brucellosis ously postulated in Uganda [6], which may influence the and proper handling of dairy products in order to control chance of brucellosis infection. However, in the pros- the disease in this population. pective study, cases increased in the months of February A limitation of the retrospective study was incomplete to March, May to August, and October to November at information from the medical records. For example, age Mbarara University teaching hospital, while at the of patients was mostly recorded as ‘adult’ instead of the Lyantonde hospital, cases increased in the months of actual age, and there was no detailed information January to February, May to July, and September to No- regarding area of residence, hence our analysis was lim- vember. This could be due to the provision of diagnostic ited. However, the missing information did not affect the reagents by our study for the period of study which en- trends analysis as we minimised this by conducting a abled diagnostic testing and case detection. prospective 1-year study. The unavailability of reagents On the other hand, the significant difference between for diagnosis did result in reduced numbers of patients the number of cases at the health facilities (p<0.001) presenting to the public hospital. We recommend that was depicted in the reduction of cases at the public the government makes these services and whatever is teaching hospital compared to the private clinic in the required to treat brucellosis more available to the health retrospective study (October to December), and the facilities in order to meet the needs of patients. numerous declines from January to February, March to May and August to October at the Mbarara teaching hospital in the prospective study. This was because there Conclusions was a lack of reagents and test kits due to budgetary The 10-year study showed that trend distribution of hu- constraints in the first half of the financial year (June to man brucellosis cases at the two health facilities varied in December), as mentioned by two health providers dur- different years, with a noticeable increase in prevalence ing the survey, which led to a considerable level of from 2010 to 2012. The prospective study confirmed this. underreporting of the disease. We suggest that teaching Diagnosis of both brucellosis and typhoid is important for and other government hospitals in endemic areas are early detection, instituting control measures and raising preferentially equipped with diagnostic facilities, equip- public awareness on prevention methods for brucellosis in ment, kits and reagents. Simple and rapid diagnostic the study area. tests such as the Rose Bengal plate test for screening for brucellosis and more specific confirmatory tests such as Competing interests the serum agglutination test are needed in endemic areas The authors declare that they have no competing interests. [23, 24], especially where most health facilities do not Authors’ contributions have laboratories that offer more advanced testing for CK was involved in the development of the concept, study design, data brucellosis. This is important for early detection, treat- collection, analysis and writing of the paper. AM and ER helped to develop the ment and control of the disease. concept, supervised the study and critically revised the paper. FM participated in the study design and data interpretation, revised the paper and approved the In the prospective study, we found that respondents final version. JB participated in the acquisition of the data, revised the paper and aged 45–60 years were less likely to have brucellosis approved the final version. BBA participated in the development of the concept, Kansiime et al. Infectious Diseases of Poverty (2015) 4:39 Page 8 of 8

study design, and the drafting and final revision of the paper. All authors read 19. Thakur SD, Kumar R, Thapliyal DC. Human brucellosis: review of an and approved the final version of the paper. under-diagnosed animal transmitted diseases. J Commun Dis. 2002;34:287–301. Acknowledgements 20. Schelling E, Diguimbaye C, et al. Brucellosis and Q-fever sero-prevalenc of The authors are grateful for the financial support from the International nomadic pastoralists and their livestock in Chad. Prev Vet Med. – Development Research Centre (IDRC), Canada, and the participating 2000;61:279 93. laboratories for granting access to the records. 21. Minas M, Minas A, Gourgulianis K, Stournara A. Epidemiological and clinical aspects of human brucellosis in Central Greece. Jpn J Infect Dis. – Author details 2007;60:362 6. 1Department of Health Policy, Planning and Management, School of Public 22. Swai ESSL. Human brucellosis: seroprevalence and risk factors related to Health, College of Health Sciences, Makerere University, P.O. Box 7072, high risk occupational groups in Tanga Municipality, Tanzania. Zoonoses – Kampala, Uganda. 2Department of Medical Microbiology, College of Health Public Health. 2009;56:183 7. Sciences, Makerere University, P.O. Box 7072, Kampala, Uganda. 3Department 23. Al Dahouk S, Tomaso H, Nockler K, Neubauer H, Frangoulidis D. — of Epidemiology and Biostatistics, School of Public Health, College of Health Laboratory-based diagnosis of brucellosis a review of the literature. Part II: – Sciences, Makerere University, P.O. Box 7072, Kampala, Uganda. 4Department serological tests for brucellosis. Clin Lab. 2003;49:577 89. of Microbiology, Mbarara University of Science and Technology, P.O. Box 24. Ruiz-Mesa JD, Sanchez-Gonzalez J, Reguera JM, Martin L, Lopez-Palmero S, 1410, Mbarara, Uganda. 5Animal Resources and Biosecurity, College of Colmenero JD. Rose Bengal test: diagnostic yield and use for the rapid Veterinary Medicine, Makerere University School of Veterinary Medicine, P.O. diagnosis of human brucellosis in emergency departments in endemic – Box 7062, Kampala, Uganda. areas. Clin Microbiol Infect. 2005;11:221 5. 25. Al Dahouk S, Tomaso H, Nockler K, Neubauer H, Frangoulidis D. — Received: 10 April 2015 Accepted: 14 July 2015 Laboratory-based diagnosis of brucellosis a review of the literature. Part II: serological tests for brucellosis. Clin Lab. 2003;49:577–89.

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